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Trade-Offs Between Burrowing and Biting Force in Fossorial Scincid Lizards?

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Trade-Offs Between Burrowing and Biting Force in Fossorial Scincid Lizards? applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Biological Journal of the Linnean Society, 2020, XX, 1–10. With 2 figures. Downloaded from https://academic.oup.com/biolinnean/advance-article-abstract/doi/10.1093/biolinnean/blaa031/5839769 by Museum National d'Histoire Naturelle user on 19 May 2020 Trade-offs between burrowing and biting force in fossorial scincid lizards? MARGOT LE GUILLOUX1, AURÉLIEN MIRALLES2, JOHN MEASEY3, BIEKE VANHOOYDONCK4, JAMES C. O’REILLY5, AURÉLIEN LOWIE6, and ANTHONY HERREL1,4,6,*, 1UMR 7179 C.N.R.S/M.N.H.N., Département Adaptations du Vivant, Bâtiment d’Anatomie Comparée, 55 rue Buffon, 75005, Paris, France 2Institut de Systématique, Evolution, Biodiversité, (UMR 7205 Muséum national d’Histoire naturelle, CNRS UPMC EPHE, Sorbonne Universités), CP30, 25 rue Cuvier 75005, Paris, France 3Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Private Bag X1, 7602 Matieland, Stellenbosch, South Africa 4Deparment of Biology, University of Antwerp, Universiteitsplein 1, B2610 Antwerpen, Belgium 5Department of Biomedical Sciences, Ohio University, Cleveland Campus, SPS-334C, Cleveland, 45701 Ohio, USA 6Department of Biology, Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium Received 27 December 2019; revised 17 February 2020; accepted for publication 19 February 2020 Trade-offs are thought to be important in constraining evolutionary divergence as they may limit phenotypic diversification. The cranial system plays a vital role in many functions including defensive, territorial, predatory and feeding behaviours in addition to housing the brain and sensory systems. Consequently, the morphology of the cranial system is affected by a combination of selective pressures that may induce functional trade-offs. Limbless, head-first burrowers are thought to be constrained in their cranial morphology as narrow heads may provide a functional advantage for burrowing. However, having a wide and large head is likely beneficial in terms of bite performance. We used 15 skink species to test for the existence of trade-offs between maximal push and bite forces, and explored the patterns of covariation between external head and body morphology and performance. Our data show that there is no evidence of a trade-off between bite and burrowing in terms of maximal force. Species that generate high push forces also generate high bite forces. Our data also show that overall head size covaries with both performance traits. However, future studies exploring trade-offs between force and speed or the energetic cost of burrowing may reveal other trade-offs. ADDITIONAL KEYWORDS: covariation – cranial system – divergence – head-first burrowers – morphology – skink. INTRODUCTION anatomical structures (Arnold, 1992; Van Damme et al., 2002, 2003). Previous studies have further suggested The phenotype of an organism reflects the selective that trade-offs may in some cases limit phenotypic pressures exerted by activities that are essential variation by constraining evolutionary divergence to its survival and its reproduction (Arnold, 1993). (Vanhooydonck et al., 2001; Levinton & Allen, 2005; Sometimes, however, the functional demands exerted Konuma & Chiba, 2007; Herrel et al., 2009). The by different performance traits may result in trade- cranial system plays a vital role in many activities offs. Indeed, functional trade-offs arise when different including defensive, territorial, predatory and feeding functions exert conflicting pressures on the same behaviours in addition to housing and protecting the brain and major sensory organs (Andrews et al., 1987; *Corresponding author. E-mail: [email protected] Cooper & Vitt, 1993; Herrel et al., 2007; Kohlsdorf © 2020 The Linnean Society of London, Biological Journal of the Linnean Society, 2020, XX, 1–10 1 2 Burrowing and Biting in Scincid Lizards Downloaded from https://academic.oup.com/biolinnean/advance-article-abstract/doi/10.1093/biolinnean/blaa031/5839769 by Museum National d'Histoire Naturelle user on 19 May 2020 et al., 2008; Dumont et al., 2016). Consequently, the burrowing force. Consequently, trade-offs between these morphology of the cranial system is affected by these two performance traits, if present, are not mediated by combined selective pressures which may potentially direct functional conflict for the optimization of single induce functional trade-offs. functional trait. Rather, burrowers can be expected to The hypothetical trade-off between biting and have narrow heads for efficient soil penetration which borrowing performance is particularly interesting may come at a cost of bite force. in limbless burrowing animals. These organisms are Here, we test for the presence of a trade-off between obligate head-first burrowers and the evolution of maximal bite force and the maximal push force in a their morphology is thought to be constrained. Indeed, range of burrowing and leaf-litter dwelling skinks. because the energy required for burrowing increases Scincid lizards represent an ideal study system as this exponentially with body and head diameter (Navas family includes a variety of ecologies and morphologies et al., 2004), having a thin body and a narrow head with quadrupedal surface-dwelling species, epigeal may provide a functional advantage for burrowing. Yet, serpentiform species with partially reduced front- and/ this is likely detrimental in terms of bite performance or hindlimbs, burrowing completely limbless species, and (Verwaijen et al., 2002; Navas et al., 2004; Herrel & a plethora of intermediate forms (Pianka & Vitt, 2003; O’Reilly, 2006; Vanhooydonck et al., 2011; Baeckens Miralles et al., 2015; Wagner et al., 2018; Bergmann & et al., 2017; Hohl et al., 2017). Maximum bite force has Morinaga, 2019). At least 15 independent evolutions of a been suggested to limit the type and size of food an serpentiform body form have taken place within the group animal can eat (Herrel et al., 1999, 2001, 2008; Aguirre (Benesh & Withers, 2002; Miralles et al., 2012) allowing et al., 2003; McBrayer & Corbin, 2007; Edwards et al., for a robust framework to test for associations between 2013). Consequently, a cranial form optimized for soil life-style, performance and morphology. Consequently, penetration may compromise the types of food an we also explore the patterns of covariation between head animal can eat and vice versa (Andrews et al., 1987; and body morphology and the two performance traits Barros et al., 2011; Baeckens et al., 2017). studied here (bite force and push force). Burrowing is a complex behaviour that remains rather poorly understood in limbless head-first burrowing vertebrates (but see for example Gaymer (1971); Gans (1973); O’Reilly et al. (1997); Teodecki et al. MATERIALS AND METHODS (1998); Navas et al. (2004); De Schepper et al. (2005)). ANIMALS The maximal push force that an animal can generate is likely important as it may allow an animal to penetrate Morphological measurements were performed on 180 a greater variety of soil types, and thus expand its individuals and performance measurements were resource base in terms of potential habitat and food obtained for 171 individuals for bite forces and 159 for resources. As limbless species burrow by recruiting push forces across 14 different species (Table 1). Animals muscles along the long axis of the body (Rieppel, 1981; were sampled between 2000 and 2017. The specimens Navas et al., 2004; Vanhooydonck et al., 2011; Hohl were adults of often unknown sex. Data were collected in et al., 2017), the diameter and size of the body should situ in the field or in the lab for species that were obtained be related to the maximal push force it can generate. through the pet trade. An additional five individuals of However, to facilitate soil penetration the width of the the species Pygomeles braconnieri from the collections of head should rather be narrow as this optimizes the the National Museum of Natural History in Paris were pressure for a given force (e.g. Measey & Herrel, 2006; used for morphological measurements. Herrel & Measey, 2010; Barros et al., 2011). Moreover, the speed by which it can penetrate the soil (and not only MORPHOMETRICS the force generated) is also likely a factor significantly contributing to the burrowing performance (Ducey Each individual was weighed using an electronic et al., 1993; Teodecki et al., 1998; Vanhooydonck et al., balance (Ohaus, ± 0.1 g). Head length, head width, 2011). Although few quantitative data exist, a previous head depth and lower jaw length were measured using study suggested the presence of a trade-off between bite a digital caliper (Mitutoyo, ± 0.01 mm) as described force and burrowing speed in a limbless skink, Acontias previously (Herrel and Holanova, 2008). The snout- percevali, mediated by the conflicting demands on vent length was measured by stretching the animals head dimensions (Vanhooydonck et al., 2011). However, along a ruler (± 1 mm). whether this is more generally the case and whether trade-offs also exist between bite force and push force remains unknown. As burrowing force is dependent MAXIMAL PUSH FORCE on the axial musculature, different anatomical traits Maximal push forces were measured in the field or in the are responsible for the generation of bite force vs. lab following the protocol described in Vanhooydonck © 2020 The Linnean Society of London, Biological Journal of the Linnean Society, 2020, XX, 1–10 © 2020 The Linnean Society of London, The Linnean
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